Distinct goal location beta frequency dynamics in hippocampus and prefrontal cortex across learning

Neural activity at goal locations contributes to learning by providing feedback on the success of preceding actions. This period engages neocortical and hippocampal networks, which serve distinct functions in reward processing and in forming associations between experience and reward. A neocortical network signature for reward feedback processing is beta oscillations (15-30 Hz). Beta oscillations are thought to coordinate distributed neural processes across brain regions. However, it is unknown whether beta oscillations coordinate hippocampal-neocortical networks during the goal period, or how their dynamics relate to learning. Here, we show that beta oscillations occur in both hippocampal CA1 and the prefrontal cortex (PFC) when rats reach goal locations in spatial navigation tasks. Despite the presence of beta oscillations in both regions after goal entry, beta activity in each region differed in spectral and temporal properties. These differences suggest that the hippocampus and PFC are weakly coupled at the beta frequency. We found that across learning, the strengths of PFC and CA1 beta oscillations were inversely related: PFC beta power increased and CA1 beta power decreased. Beta burst properties in PFC also had an inverse relationship to those of hippocampal sharp wave-ripples (SWRs), a prominent hippocampal process required for learning. We found a subset of PFC neurons modulated by both beta and hippocampal SWRs, which had distinct task-related firing patterns. Our results suggest that during outcome processing at goal locations, the neocortex and hippocampus are locally modulated at the beta frequency and then become coordinated for memory-related processes during SWRs.